TY - JOUR
T1 - A pendulum of induction between the epiblast and extra-embryonic endoderm supports post-implantation progression
AU - Vrij, Erik J.
AU - Scholte Op Reimer, Yvonne S.
AU - Fuentes, Laury Roa
AU - Guerreiro, Isabel Misteli
AU - Holzmann, Viktoria
AU - Aldeguer, Javier Frias
AU - Sestini, Giovanni
AU - Koo, Bon Kyoung
AU - Kind, Jop
AU - van Blitterswijk, Clemens A.
AU - Rivron, Nicolas C.
N1 - Funding Information:
The authors thank Christian Schröter for providing the Gata6-Venus mouse ES cells; Valerie Prideaux, Jodi Garner and Janet Rossant for providing the F4 mouse TS cell lines; Anna-Katerina Hadjantonakis for providing the Pdgfrα-h2b-gfp mouse ES cells; and Single Cell Discoveries for providing de-multiplexed sequencing files. The Oncode Institute is partially funded by the KWF Kankerbestrijding.
Funding Information:
This project has received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation program (2015 ERC-AdG number 694801-ORCHESTRATE) and from the Stichting De Weijerhorst (‘Synthetic Embryos’ PC0089). N.C.R. is funded by the European Research Council (2020 ERC-CoG number 101002317-BLASTOID). V.H. is funded by a Boehringer Ingelheim Fonds PhD fellowship. J.K. is funded by the European Research Council (2016 ERC-StG 678423-EpiID). I.M.G. is supported by a European Molecular Biology Organization Long-Term Fellowship (ALTF1214-2016), by the Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (P400PB_186758) and by a Nederlandse Organisatie voor Wetenschappelijk Onderzoek-ZonMW Veni grant (VI.Veni.202.073). Open access funding provided by the Institute of Molecular Biotechnology of the Austrian Academy of Sciences. Deposited in PMC for immediate release.
Funding Information:
The authors thank Christian Schröter for providing the Gata6-Venus mouse ES cells; Valerie Prideaux, Jodi Garner and Janet Rossant for providing the F4 mouse TS cell lines; Anna-Katerina Hadjantonakis for providing the Pdgfrα-h2b-gfp mouse ES cells; and Single Cell Discoveries for providing de-multiplexed sequencing files. The Oncode Institute is partially funded by the KWF Kankerbestrijding. This project has received funding from the European Research Council under the European Union’s Horizon 2020 research and innovation program (2015 ERC-AdG number 694801-ORCHESTRATE) and from the Stichting De Weijerhorst (‘Synthetic Embryos’ PC0089). N.C.R. is funded by the European Research Council (2020 ERC-CoG number 101002317-BLASTOID). V.H. is funded by a Boehringer Ingelheim Fonds PhD fellowship. J.K. is funded by the European Research Council (2016 ERC-StG 678423-EpiID). I.M.G. is supported by a European Molecular Biology Organization Long-Term Fellowship (ALTF1214-2016), by the Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (P400PB_186758) and by a Nederlandse Organisatie voor Wetenschappelijk Onderzoek-ZonMW Veni grant (VI.Veni.202.073). Open access funding provided by the Institute of Molecular Biotechnology of the Austrian Academy of Sciences. Deposited in PMC for immediate release.
Publisher Copyright:
© 2022. Published by The Company of Biologists Ltd.
PY - 2022/10/15
Y1 - 2022/10/15
N2 - Embryogenesis is supported by dynamic loops of cellular interactions. Here, we create a partial mouse embryo model to elucidate the principles of epiblast (Epi) and extra-embryonic endoderm co-development (XEn). We trigger naive mouse embryonic stem cells to form a blastocyst-stage niche of Epi-like cells and XEn-like cells (3D, hydrogel free and serum free). Once established, these two lineages autonomously progress in minimal medium to form an inner pro-amniotic-like cavity surrounded by polarized Epi-like cells covered with visceral endoderm (VE)-like cells. The progression occurs through reciprocal inductions by which the Epi supports the primitive endoderm (PrE) to produce a basal lamina that subsequently regulates Epi polarization and/or cavitation, which, in return, channels the transcriptomic progression to VE. This VE then contributes to Epi bifurcation into anterior- and posterior-like states. Similarly, boosting the formation of PrE-like cells within blastoids supports developmental progression. We argue that self-organization can arise from lineage bifurcation followed by a pendulum of induction that propagates over time.
AB - Embryogenesis is supported by dynamic loops of cellular interactions. Here, we create a partial mouse embryo model to elucidate the principles of epiblast (Epi) and extra-embryonic endoderm co-development (XEn). We trigger naive mouse embryonic stem cells to form a blastocyst-stage niche of Epi-like cells and XEn-like cells (3D, hydrogel free and serum free). Once established, these two lineages autonomously progress in minimal medium to form an inner pro-amniotic-like cavity surrounded by polarized Epi-like cells covered with visceral endoderm (VE)-like cells. The progression occurs through reciprocal inductions by which the Epi supports the primitive endoderm (PrE) to produce a basal lamina that subsequently regulates Epi polarization and/or cavitation, which, in return, channels the transcriptomic progression to VE. This VE then contributes to Epi bifurcation into anterior- and posterior-like states. Similarly, boosting the formation of PrE-like cells within blastoids supports developmental progression. We argue that self-organization can arise from lineage bifurcation followed by a pendulum of induction that propagates over time.
KW - Blastoids
KW - Embryonic stem cells
KW - Extra-embryonic endoderm/epiblast rosette
KW - Post-implantation development
KW - Primitive endoderm
KW - Pro-amniotic cavity
UR - http://www.scopus.com/inward/record.url?scp=85136226593&partnerID=8YFLogxK
U2 - 10.1242/dev.192310
DO - 10.1242/dev.192310
M3 - Article
C2 - 35993866
AN - SCOPUS:85136226593
SN - 0950-1991
VL - 149
JO - Development (Cambridge, England)
JF - Development (Cambridge, England)
IS - 20
M1 - dev192310
ER -